Defence gene expression and phloem quality contribute to mesophyll and phloem resistance to aphids in wild barley

Abstract Aphids, including the bird cherry-oat aphid (Rhopalosiphum padi), are significant agricultural pests. The wild relative of barley, Hordeum spontaneum 5 (Hsp5), has been described to be partially resistant to R. padi, with this resistance proposed to involve higher thionin and lipoxygenase gene expression. However, the specificity of this resistance to aphids and its underlying mechanistic processes are unknown. In this study, we assessed the specificity of Hsp5 resistance to aphids and analysed differences in aphid probing and feeding behaviour on Hsp5 and a susceptible barley cultivar (Concerto). We found that partial resistance in Hsp5 to R. padi extends to two other aphid pests of grasses. Using the electrical penetration graph technique, we show that partial resistance is mediated by phloem- and mesophyll-based resistance factors that limit aphid phloem ingestion. To gain insight into plant traits responsible for partial resistance, we compared non-glandular trichome density, defence gene expression, and phloem composition of Hsp5 with those of the susceptible barley cultivar Concerto. We show that Hsp5 partial resistance involves elevated basal expression of thionin and phytohormone signalling genes, and a reduction in phloem quality. This study highlights plant traits that may contribute to broad-spectrum partial resistance to aphids in barley.

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Partial-resistance against aphids in wild barley involves phloem and mesophyll-based defences

10.1101/502476 ◽

2018 ◽

Author(s):

Daniel J Leybourne ◽

Tracy A Valentine ◽

Jean AH Robertson ◽

Estefania Pérez-Fernández ◽

Angela M Main ◽

...

Keyword(s):

Gene Expression ◽

Amino Acid ◽

Amino Acid Composition ◽

Acid Composition ◽

Partial Resistance ◽

Management Practices ◽

Vascular Tissue ◽

Wild Barley ◽

Agricultural Pests ◽

Electrical Penetration Graph

AbstractAphids, including the bird cherry-oat aphid (Rhopalosiphum padi), are significant agricultural pests. Aphid populations are typically controlled using insecticides, but there is increasing demand for more sustainable pest management practices. The wild relative of barley, Hordeum spontaneum 5 (Hsp5) has been described as partially-resistant to R. padi. Partial-resistance is proposed to involve higher thionin and lipoxygenase gene expression. However, the underlying mechanistic processes are unknown. In this study we compared Hsp5 with a susceptible cultivar of barley (Concerto) to test the extent to which partial-resistance affects aphid fitness. We used the electrical penetration graph technique to monitor R. padi feeding patterns to elucidate the tissue location of partial-resistance factors alongside molecular and biochemical analyses to identify potential mechanisms. We show that partial-resistance in Hsp5 extends to three aphid species and is mediated by phloem/mesophyll-based factors, leading to a three-fold increase in the time aphids take to establish sustained phloem ingestion. Partial-resistance likely involves elevated expression of defence and phytohormone genes alongside altered phloem amino acid composition. Further work is required to establish the function of these traits, however this study highlights plant tissues which are important in conferring broad-spectrum partial-resistance against aphids in barley.HighlightPartial-resistance against aphids in wild barley is based in the mesophyll and vascular tissue and is potentially associated with higher basal defence gene expression and altered phloem amino acid composition.

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Partial-resistance against aphids in wild barley reduces the oviposition success of the generalist parasitoid, Aphidius colemani Viereck

10.1101/653113 ◽

2019 ◽

Cited By ~ 1

Author(s):

Daniel. J. Leybourne ◽

Tracy. A. Valentine ◽

Jorunn. I. B. Bos ◽

Alison. J. Karley

Keyword(s):

Plant Resistance ◽

Partial Resistance ◽

Rhopalosiphum Padi ◽

Hordeum Spontaneum ◽

Unintended Consequences ◽

Cereal Aphids ◽

Agricultural Pests ◽

Modern Cultivar ◽

Aphidius Colemani ◽

Aphid Control

AbstractAphids are significant agricultural pests of cereal crops with a worldwide distribution. The control of aphids in agricultural systems is currently heavily reliant on insecticidal compounds, but it is becoming increasingly apparent that chemical-based control of agricultural pests has far-reaching unintended consequences on agro-ecosystems. As a result, more sustainable means of aphid control are becoming increasingly desirable. Potential options include increasing plant resistance against aphids, promoting biocontrol, and the combined use of both strategies. When used together it is important to understand how, and to what extent, increased plant resistance against aphids affects the success of biocontrol agents. In this current study, we examine how partial-resistance against cereal aphids in a wild relative of barley, Hordeum spontaneum 5 (Hsp5), affects the success of the common parasitoid of cereal aphids, Aphidius colemani. We show that the parasitism success of A. colemani attacking nymphs of the bird cherry-oat aphid, Rhopalosiphum padi, contained on Hsp5 is reduced compared with the parasitism success of wasps attacking R. padi nymphs feeding on a susceptible modern cultivar of barley, H. vulgare cv. Concerto. Explanta parasitism assays showed that the in parasitoid success is a direct effect of the plant environment (such as differential architectural traits), rather than an indirect effect dur to a decrease in aphid suitability resulting from increased resistance against aphids in Hsp5. Our study highlights the importance of understanding the direct and indirect effects of plant resistance against aphids on biocontrol strategies.

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An aphid effector promotes barley susceptibility through suppression of defence gene expression

Journal of Experimental Botany ◽

10.1093/jxb/eraa043 ◽

2020 ◽

Vol 71 (9) ◽

pp. 2796-2807 ◽

Cited By ~ 1

Author(s):

Carmen Escudero-Martinez ◽

Patricia A Rodriguez ◽

Shan Liu ◽

Pablo A Santos ◽

Jennifer Stephens ◽

...

Keyword(s):

Gene Expression ◽

Sequence Similarity ◽

Rhopalosiphum Padi ◽

Functional Characterization ◽

Aphid Species ◽

Transgenic Barley ◽

Defence Gene Expression ◽

Hormone Signalling ◽

Plant Susceptibility

Abstract Aphids secrete diverse repertoires of effectors into their hosts to promote the infestation process. While ‘omics’ approaches facilitated the identification and comparison of effector repertoires from a number of aphid species, the functional characterization of these proteins has been limited to dicot (model) plants. The bird cherry-oat aphid Rhopalosiphum padi is a pest of cereal crops, including barley. Here, we extend efforts to characterize aphid effectors with regard to their role in promoting susceptibility to the R. padi–barley interaction. We selected three R. padi effectors based on sequence similarity to previously characterized Myzus persicae effectors and assessed their subcellular localization, expression, and role in promoting plant susceptibility. Expression of R. padi effectors RpC002 and Rp1 in transgenic barley lines enhanced plant susceptibility to R. padi but not M. persicae, for which barley is a poor host. Characterization of Rp1 transgenic barley lines revealed reduced gene expression of plant hormone signalling genes relevant to plant–aphid interactions, indicating that this effector enhances susceptibility by suppressing plant defences in barley. Our data suggest that some aphid effectors specifically function when expressed in host species, and feature activities that benefit their corresponding aphid species.

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An aphid effector promotes barley susceptibility through suppression of defence gene expression

10.1101/639476 ◽

2019 ◽

Author(s):

Carmen Escudero-Martinez ◽

Patricia A. Rodriguez ◽

Pablo A. Santos ◽

Jennifer Stephens ◽

Jorunn I.B. Bos

Keyword(s):

Gene Expression ◽

Rhopalosiphum Padi ◽

Functional Characterization ◽

Aphid Species ◽

Subcellular Localisation ◽

Transgenic Barley ◽

Defence Gene Expression ◽

Hormone Signalling ◽

Plant Susceptibility

AbstractAphids secrete diverse repertoires of effectors into their hosts to promote the infestation process. While “omics”-approaches facilitated the identification and comparison of effector repertoires from a number of aphid species, the functional characterization of these proteins has been limited to dicot (model) plants. The bird cherry-oat aphid Rhopalosiphum padi is a pest of cereal crops, including barley. Here, we extended efforts to characterize aphid effectors with regards to their role in promoting susceptibility to the R. padi-barley interaction. We selected 3 R. padi effectors based on sequences similarity to previously characterized M. persicae effectors and assessed their subcellular localisation, expression, and role in promoting plant susceptibility. Expression of R. padi effectors RpC002 and Rp1 in transgenic barley lines enhanced plant susceptibility to R. padi but not M. persicae, for which barley is a poor host. Characterization of Rp1 transgenic barley lines revealed reduced gene expression of plant hormone signalling genes relevant to plant-aphid interactions, indicating this effector enhances susceptibility by suppressing plant defences in barley. Our data suggests that some aphid effectors specifically function when expressed in host species, and feature activities that benefit their corresponding aphid species.

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A fitness cost resulting fromHamiltonella defensainfection is associated with altered probing and feeding behaviour inRhopalosiphum padi

10.1101/652974 ◽

2019 ◽

Author(s):

Daniel. J. Leybourne ◽

Tracy. A. Valentine ◽

Jorunn. I. B. Bos ◽

Alison. J. Karley

Keyword(s):

Host Plant ◽

Plant Tissue ◽

Feeding Behaviour ◽

Rhopalosiphum Padi ◽

Physiological Mechanism ◽

Fold Increase ◽

Hordeum Spontaneum ◽

Plant Responses ◽

Electrical Penetration Graph ◽

Aphid Feeding

AbstractAphids frequently associate with facultative endosymbiotic bacteria which influence aphid physiology in myriad ways. Endosymbiont infection can increase aphid resistance against parasitoids and pathogens, modulate plant responses to aphid feeding, and promote aphid virulence. These endosymbiotic relationships can also decrease aphid fitness in the absence of natural enemies or when feeding on less suitable plant types. Here, we use the Electrical Penetration Graph (EPG) technique to monitor feeding behaviour of four genetically-similar clonal lines of a cereal-feeding aphid,Rhopalosiphum padi, differentially infected (+/−) with the facultative protective endosymbiont,Hamiltonella defensa, to understand how physiological processes at the aphid-plant interface are affected by endosymbiont infection. Endosymbiont-infected aphids exhibited altered probing and feeding patterns compared with uninfected aphids, characterised by a two-fold increase in the number of plant cell punctures, a 50% reduction in the duration of each cellular puncture, and a greater probability of achieving sustained ingestion of plant phloem. Feeding behaviour was altered further by host plant identity: endosymbiont-infected aphids spent less time probing into plant tissue, required twice as many probes into plant tissue to reach plant phloem, and showed a 44% reduction in phloem ingestion when feeding on the partially-resistant wild relative of barley,Hordeum spontaneum5, compared with a commercial barley cultivar. These observations might explain reduced growth ofH. defensa-infected aphids on the former host plant. This study is the first to demonstrate a physiological mechanism at the aphid-plant interface contributing to endosymbiont effects on aphid fitness on different quality plants through altered aphid feeding behaviour.SummaryReduced performance of aphids infected with a common facultative endosymbiont on poor quality plants may be explained by changes in aphid probing behaviour and decreased phloem sap ingestion.

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The jasmonoyl‐isoleucine receptor CORONATINE INSENSITIVE1 suppresses defence gene expression in Arabidopsis roots independently of its ligand

The Plant Journal ◽

10.1111/tpj.15372 ◽

2021 ◽

Author(s):

Louisa Ulrich ◽

Johanna Schmitz ◽

Corinna Thurow ◽

Christiane Gatz

Keyword(s):

Gene Expression ◽

Defence Gene Expression

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Gene body methylation mediates epigenetic inheritance of plant traits

10.1101/2021.03.15.435374 ◽

2021 ◽

Cited By ~ 1

Author(s):

Zaigham Shahzad ◽

Jonathan D. Moore ◽

Daniel Zilberman

Keyword(s):

Gene Expression ◽

Flowering Time ◽

Cytosine Methylation ◽

Plant Traits ◽

Phenotypic Diversity ◽

Strong Association ◽

Epigenetic Inheritance ◽

Evolutionary Significance ◽

Gene Body ◽

Gene Body Methylation

AbstractCytosine methylation is an epigenetically heritable DNA modification common in plant and animal genes, but the functional and evolutionary significance of gene body methylation (gbM) has remained enigmatic. Here we show that gbM enhances gene expression in Arabidopsis thaliana. We also demonstrate that natural gbM variation influences drought and heat tolerance and flowering time by modulating gene expression, including that of Flowering Locus C (FLC). Notably, epigenetic variation accounts for as much trait heritability in natural populations as DNA sequence polymorphism. Furthermore, we identify gbM variation in numerous genes associated with environmental variables, including a strong association between flowering time, spring atmospheric NO2 – a by-product of fossil fuel burning – and FLC epialleles. Our study demonstrates that gbM is an important modulator of gene expression, and its natural variation fundamentally shapes phenotypic diversity in plant populations. Thus, gbM provides an epigenetic basis for adaptive evolution independent of genetic polymorphism.

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Proteomic analyses of defence gene expression in a model tomato‐Verticillium pathosystem

The FASEB Journal ◽

10.1096/fasebj.23.1_supplement.lb242 ◽

2009 ◽

Vol 23 (S1) ◽

Author(s):

Jane Robb ◽

Barbara Lee ◽

Alex Kurosky ◽

Ross N. Nazar

Keyword(s):

Gene Expression ◽

Defence Gene Expression ◽

Proteomic Analyses

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Expression of Thioredoxin/Thioredoxin Reductase System Genes in Aphid-Challenged Maize Seedlings

International Journal of Molecular Sciences ◽

10.3390/ijms21176296 ◽

2020 ◽

Vol 21 (17) ◽

pp. 6296

Author(s):

Hubert Sytykiewicz ◽

Iwona Łukasik ◽

Sylwia Goławska ◽

Iwona Sprawka ◽

Artur Goławski ◽

...

Keyword(s):

Redox Homeostasis ◽

Rhopalosiphum Padi ◽

Thioredoxin Reductase ◽

Redox Balance ◽

Electrical Penetration Graph ◽

Metopolophium Dirhodum ◽

Transcriptional Reprogramming ◽

Maize Varieties ◽

Maize Plants ◽

Thioredoxin Reductases

Thioredoxins (Trxs) and thioredoxin reductases (TrxRs) encompass a highly complex network involved in sustaining thiol-based redox homeostasis in plant tissues. The purpose of the study was to gain a new insight into transcriptional reprogramming of the several genes involved in functioning of Trx/TrxR system in maize (Zea mays L.) seedlings, exposed to the bird cherry-oat aphid (Rhopalosiphum padi L.) or the rose-grass aphid (Metopolophium dirhodum Walk.) infestation. The biotests were performed on two maize genotypes (susceptible Złota Karłowa and relatively resistant Waza). The application of real-time qRT-PCR technique allowed to identify a molecular mechanism triggered in more resistant maize plants, linked to upregulation of thioredoxins-encoding genes (Trx-f, Trx-h, Trx-m, Trx-x) and thioredoxin reductase genes (Ftr1, Trxr2). Significant enhancement of TrxR activity in aphid-infested Waza seedlings was also demonstrated. Furthermore, we used an electrical penetration graph (EPG) recordings of M. dirhodum stylet activities in seedlings of the two studied maize varieties. Duration of phloem phase (E1 and E2 models) of rose-grass aphids was about three times longer while feeding in Waza plants, compared to Złota Karłowa cv. The role of activation of Trx/TrxR system in maintaining redox balance and counteracting oxidative-induced damages of macromolecules in aphid-stressed maize plants is discussed.

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